V.J.T. van Ginneken

Eel migration to the Sargasso: remarkably high swimming efficiency and low energy costs

SUMMARY One of the mysteries of the animal kingdom is the long-distance migration (5000–6000 km) of the European eel Anguilla anguilla L. from the coasts of Europe to its spawning grounds in the Sargasso Sea. The only evidence for the location of the spawning site of the European eel in the Sargasso Sea is the discovery by Johannes Schmidt at the beginning of the previous century of the smallest eel larvae (leptocephali) near the Sargasso Sea. For years it has been questioned whether the fasting eels have sufficient energy reserves to cover this enormous distance. We have tested Schmidts theory by placing eels in swim tunnels in the laboratory and allowing them to make a simulated migration of 5500 km. We find that eels swim 4–6 times more efficiently than non-eel-like fish. Our findings are an important advance in this field because they remove a central objection to Schmidts theory by showing that their energy reserves are, in principle, sufficient for the migration. Conclusive proof of the Sargasso Sea theory is likely to come from satellite tracking technology.

Eel fat stores are enough to reach the Sargasso

It has long been assumed that the European eel (Anguilla anguilla) migrates to the Sargasso Sea — a region of the Atlantic Ocean between the Azores and the West Indies — to spawn1,2,3. During the past decade, however, the number of glass eels has inexplicably dropped4, and it has been suggested that a shortage of fat stores in adults, resulting from diminished food resources for juveniles in inland waters, may prevent the starving silver eels from reaching the spawning grounds4,5,6. But we find that the energetic cost of the 6,000-km migration is actually quite low, with 60% of the fat store remaining available for the developing gonads.It has long been assumed that the European eel (Anguilla anguilla) migrates to the Sargasso Sea — a region of the Atlantic Ocean between the Azores and the West Indies — to spawn. During the past decade, however, the number of glass eels has inexplicably dropped, and it has been suggested that a shortage of fat stores in adults, resulting from diminished food resources for juveniles in inland waters, may prevent the starving silver eels from reaching the spawning grounds. But we find that the energetic cost of the 6,000-km migration is actually quite low, with 60% of the fat store remaining available for the developing gonads.

PCBs and the energy cost of migration in the European eel (Anguilla anguilla L.)

The effect of polychlorinated biphenyls (PCBs) on the energy consumption of fasting silver European eel (Anguilla anguilla L.) was studied over a 27-day period during which the animals were at rest or were swimming 800 km in Blazka swim tunnels. Three-year-old female hatchery eels (silver stage) between 73 and 80 cm long weighing around 1 kg were dosed intraperitoneally with PCBs at a nominal dosage of 10x the consumption standard as a mixture representative for planar (7 microg PCB126/kg eel), non-planar (5 mg PCB153/kg eel) and metabolizable PCBs (50 microg PCB77/kg eel) found in wild eel, or only with the vehicle (corn oil, 10 ml/kg eel). Four major observations were made: (1) PCB-exposed animals lose less weight compared to their unexposed controls; (2) PCB-concentrations on a lipid basis are 2.8-14 times higher in swimming compared to resting animals; (3) the standard metabolic rate is significantly lower in the PCB-exposed animals than in unexposed controls. In addition, PCB-exposure significantly reduces oxygen consumption during swimming, and starting at 400 km (18 days) this effect increases with time; (4) the relative spleen and liver weight significantly increased in the PCB-swim animals but not in the PCB-rest animals. The swimming animals lost about 75% more weight compared to resting animals and had about 50% lower plasma fat content. Hematocrit, haemoglobin, plasma pH, ion levels (sodium and potassium), and plasma lactate were not affected by PCB-exposure or swimming. Apparently, the current levels of PCBs and other dioxin-like compounds may seriously impair the reproduction of the European eel.

Physiology: Eel fat stores are enough to reach the Sargasso

It has long been assumed that the European eel (Anguilla anguilla) migrates to the Sargasso Sea — a region of the Atlantic Ocean between the Azores and the West Indies — to spawn1,2,3. During the past decade, however, the number of glass eels has inexplicably dropped4, and it has been suggested that a shortage of fat stores in adults, resulting from diminished food resources for juveniles in inland waters, may prevent the starving silver eels from reaching the spawning grounds4,5,6. But we find that the energetic cost of the 6,000-km migration is actually quite low, with 60% of the fat store remaining available for the developing gonads.It has long been assumed that the European eel (Anguilla anguilla) migrates to the Sargasso Sea — a region of the Atlantic Ocean between the Azores and the West Indies — to spawn. During the past decade, however, the number of glass eels has inexplicably dropped, and it has been suggested that a shortage of fat stores in adults, resulting from diminished food resources for juveniles in inland waters, may prevent the starving silver eels from reaching the spawning grounds. But we find that the energetic cost of the 6,000-km migration is actually quite low, with 60% of the fat store remaining available for the developing gonads.

Silvering of European eel ( Anguilla anguilla L.): seasonal changes of morphological and metabolic parameters

The transformation of yellow eel into silver eel is called `silvering?, and takes place prior to migration. We found the sedentary yellow phase in spring, the migratory silver phase in autumn, while August was a cross-over month. We used principal component analysis (PCA) to characterise the morphological and physiological changes that accompany silvering in the European eel (Anguilla anguilla L.). Silvering is positively related to external parameters such as eye size, internal maturation parameters like GSI, vitellogenine (VIT), and blood-substrates such as phospholipids, Free Fatty Acids (FFA), and cholesterol. The Hepatosomatic Index was not significantly different between yellow and silver groups. In contrast, a significant difference was observed for parameters of body constitution (fat, protein, dry matter) between yellow and silver stages. Furthermore, the process of silvering is accompanied with increased levels of cortisol in autumn, which plays a role in mobilisation of metabolic energy from body stores towards migratory activity and gonadal growth. Based on Principal Component Analysis (PCA) with physiological, morphological and endocrinological parameters, it is concluded that during the process of silvering, several developmental stages can be recognised, with a timeframe of the premigratory sedentary yellow phase from April until July, August is a cross-over month, and the migratory silver phase is found from September until November.

Seasonal Evolution and Individual Differences in Silvering Eels from Different Locations

Silvering is a requirement for downstream migration and reproduction. It marks the end of the growth phase and the onset of sexual maturation. This true metamorphosis involves a number of different physiological functions (osmoregulatory, reproductive), which prepare the eel for the long return trip to the Sargasso Sea. Unlike smoltification in salmonids, silvering of eels is largely unpredictable. It occurs at various ages (females: 4–20 years; males 2–15 years) and sizes (body length of females: 50–100 cm; males: 35–46 cm) (Tesch 2003). It is most common when studying eels, to separate individuals into two groups, yellow (resident) and silver (presumably migrant), and to compare the physiological profiles between the two. Basic knowledge was obtained in this way and we will first review what is known about these two stages. Because of the difficulty of getting individuals while they are in the process of metamorphosing, little is known about the dynamics of the silvering process. Here we present new information on the triggers, duration and succession of events up to

Neurotransmitter levels and energy status in brain of fish species with and without the survival strategy of metabolic depression

Abstract The effects of anoxia were studied in the whole brain of three fish species, each with a specific metabolic strategy for anoxic survival. Goldfish (Carassius auratus) combine a lactate to ethanol conversion with a metabolic depression, tilapia (Oreochromis mossambicus) use an anaerobic glycolysis with the strategy of metabolic depression, and carp (Cyprinus carpio) use an increased anaerobic glycolysis for energy production. Tilapia and carp were exposed to anoxia until they lost equilibrium and exhibited escape reactions, this occurred after 2 hours of anoxia for tilapia and 30 minutes of anoxia for carp. Goldfish were exposed to a selected period of 8 hours anoxia. The energy status and neurotransmitter (amino acid) levels in whole brain tissue were measured after anoxia exposure. The energy status was affected in all three groups exposed to anoxia. Lactic acid levels increased five- to six-fold in all three groups. No direct correlation was observed between energy status and survival strategy. Remarkably, the changes in the amino acid patterns in whole fish brains show the greatest changes in the anoxia-tolerant goldfish, an intermediate pattern in tilapia, and nearly no changes in the anoxia-intolerant carp. The changes in amino acid are probably dependent on the period of anoxia exposure. For goldfish, the lactate-ethanol conversion primarily determines anoxic survival, but the strategy of metabolic depression observed in goldfish and tilapia may contribute secondarily to anoxic tolerance. It is hypothesized that a decrease of excitatory neurotransmitters (mainly glutamate), in combination with an increase of inhibitory neurotransmitters (mainly GABA), may contribute to the process of metabolic depression and prolong survival.

Gynogenesis in common carp (Cyprinus carpio L.). III. The effects of inbreeding on gonadal development of heterozygous and homozygous gynogenetic offspring

Abstract The gonad development and fertility were compared for three offspring groups produced by full-sib mating (FS group: F = 0.25), gynogenesis by retention of the second polar body (2PB group; F unknown) and gynogenesis by endomitosis (EM group: F = 1), using the same common carp female. 2PB offspring were all female, but the homozygous EM offspring consisted of 50% males and intersexes which were homozygous for a recessive mutant sex-determining gene. Another mutant, affecting pigmentation in eggs, was likewise detected in the EM offspring but not in the 2PB offspring. The variation in body weight, gonad weight and egg size in each group increased with increasing degree of inbreeding. FS and 2PB offspring were comparable in mean gonadal development, but gonads from homozygous gynogenetic carp were often retarded. The ovulation response significantly decreased with increasing levels of inbreeding. Yields of normal fry were reduced in crosses involving milt from FS males and eggs from FS and 2PB females as compared with crosses with eggs or milt from EM animals. FS eggs fertilized with EM milt gave significantly better yields of normal fry than any other group. Taken together these results suggest that 2PB gynogenetic offspring are largely heterozygous for many deleterious genes affecting reproduction. In contrast, homozygous EM offspring display considerable inbreeding depression in gonad development but recessive lethal genes are excluded from the genepool.

Phosphorylation state of red and white muscle in tilapia during graded hypoxia: an in vivo31P-NMR study

The aim of this study was to measure the energetic consequences of hypoxia in different types of skeletal muscle within a single tilapia species ( n = 5). To that aim, 81.0 MHz31P-nuclear magnetic resonance (NMR) spectra were collected, alternately, from three surface coils placed adjacent to the tissues of interest (dorsal white muscle, ventral white muscle, and lateral red muscle) during a graded hypoxia load over 6 h followed by a 5-h recovery period. The fish were contained in a flow cell, enabling us full control of the oxygen content of the bathing medium. The intracellular pH and the concentrations of ATP, phosphocreatine (PCr), and Pi were determined from the NMR spectra. For normoxia, biochemical differences for [γ-ATP], [PCr], and [sugar phosphates] (SP) were observed between all three locations, especially between the red and white muscle. During hypoxia stress, loss of phosphorylated compounds (PCr+Pi+SP) was observed at all locations but was the most severe in red muscle. When the aerobic (respirometry) and anaerobic (31P-NMR) ATP production via an energy balance are compared, flexible metabolic depression is demonstrated during anaerobioses. It is concluded that control of the aerobic and anaerobic component of metabolism during metabolic depression is independent of each other.The aim of this study was to measure the energetic consequences of hypoxia in different types of skeletal muscle within a single tilapia species (n = 5). To that aim, 81.0 MHz (31)P-nuclear magnetic resonance (NMR) spectra were collected, alternately, from three surface coils placed adjacent to the tissues of interest (dorsal white muscle, ventral white muscle, and lateral red muscle) during a graded hypoxia load over 6 h followed by a 5-h recovery period. The fish were contained in a flow cell, enabling us full control of the oxygen content of the bathing medium. The intracellular pH and the concentrations of ATP, phosphocreatine (PCr), and P(i) were determined from the NMR spectra. For normoxia, biochemical differences for [gamma-ATP], [PCr], and [sugar phosphates] (SP) were observed between all three locations, especially between the red and white muscle. During hypoxia stress, loss of phosphorylated compounds (PCr+P(i)+SP) was observed at all locations but was the most severe in red muscle. When the aerobic (respirometry) and anaerobic ((31)P-NMR) ATP production via an energy balance are compared, flexible metabolic depression is demonstrated during anaerobioses. It is concluded that control of the aerobic and anaerobic component of metabolism during metabolic depression is independent of each other.

Direct calorimetry of aquatic animals: Automated and computerized data-acquisition system for simultaneous direct and indirect calorimetry

Abstract A system for computerized registration of heat production data and oxygen tension values of a differential 1 litre flow-through microcalorimeter (Setaram GF 108) is described. The linked values of oxygen concentration and heat production data were simultaneously stored on a computer. The aerobic and total heat production rates were thus measured of goldfish ( Carassius auratus L.) during normoxia, hypoxia and anoxia exposure. Incidentally, a partial anaerobic response was observed in goldfish during normoxia. During severe hypoxia and anoxia, goldfish respond with a reduction of the metabolic rate and a strong increase of anaerobic heat production. From the linked oxygen consumption and heat production data, the oxycaloric equivalent was calculated. The described system enables us to study continuously the effects of environmental factors on the metabolic rate of aquatic organisms.